The next season saw Cloutier break into stardom, as he scored 60 goals to begin a streak of four seasons of at least 56 goals. In 1976–77 season, he scored 66 goals and 141 points to lead the WHA in scoring, adding 14 goals and 13 assists in 17 playoff games to lead the Nordiques to their only AVCO Cup championship. His best goal scoring season came in the WHA's final season of 1978–79, when he scored 75 goals, at the time the third highest total in professional history.[citation needed]

Prior to the WHA's merger with the NHL in 1979, Cloutier's NHL rights belonged to the Chicago Black Hawks, which had selected him in the 1976 NHL Amateur Draft. The incoming WHA teams had a maximum of four "priority selections", up to two skaters and two goaltenders, that they could protect from being reclaimed by the NHL team that held their rights. In order to save their priority selections for defencemen Paul Baxter and Garry Lariviere, Quebec traded its first round draft choice (which would turn into future superstar Denis Savard) to Chicago in order to retain Cloutier. He proved to be a consistent scorer in the NHL, scoring 42 goals in 1979–80, and, although he was slowed by injuries, 37 and 28 goals his last two full seasons with the Nordiques.

In 1983 Cloutier's time in Quebec came to an end as he was traded to the Buffalo Sabres in exchange for Tony McKegney, André Savard, and Jean-François Sauvé. In Buffalo he reportedly clashed with Sabres' coach Scotty Bowman, who had a long history of benching offensive players whom he felt were not paying sufficient attention to defensive play, and although he scored a credible 24 goals and 60 points in his only full season for the Sabres, he was sent to the minor leagues the next year, retiring thereafter at the age of 28.

Cloutier retired as the fourth leading scorer in WHA history with 283 goals, 283 assists and 566 points in 369 games, adding 33 goals and 30 assists in 48 playoff games. In 317 NHL games, he scored 344 points.